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Invasion history of Caprella scaura Templeton, 1836 (Amphipoda: Caprellidae) in the Iberian Peninsula: multiple introductions revealed by mitochondrial sequence data

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Abstract

The caprellid Caprella scaura, native to the western Indian Ocean, is one striking example of a successful invader. It was first recorded in the Iberian Peninsula in Gerona (north-eastern coast of Spain), in 2005, and has recently been reported throughout the Mediterranean and Atlantic coasts of this region. The most likely vector of introduction and distribution is within the hull-fouling community on recreational craft. However, beyond the dates of detection, the introduction history of C. scaura remains unclear. Direct sequencing of mitochondrial DNA (cytochrome c oxidase subunit I) was used to compare genetic composition in native and introduced populations in order to infer the invasion history of this species. In addition, 18S rDNA sequences were used to resolve phylogenetic relationships within this species and with the morphologically closest species Caprella californica and Caprella scauroides. The high genetic divergence and population subdivision found between non-native Iberian populations together with a high level of genetic diversity in some populations indicate multiple geographical sources and introduction points for this caprellid. Our data suggest that Iberian populations may derive from at least two sources: (1) Pacific Australian, and (2) Indian Ocean, either directly, or, more likely, through stepping-stone events from central Mediterranean population(s). Atlantic Iberian populations seem to be the most recently established populations. On the other hand, this is the first study providing molecular evidence confirming C. scaura, C. californica and C. scauroides as distinct species. It also provides strong molecular evidence that C. scaura typica and C. scaura scaura correspond to the same subspecies, and the Japanese C. scaura diceros and the Chilean C. scaura spinirostris could merit specific rank.

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References

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Contr 19:716–723

    Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Aoki M, Kikuchi T (1990) Caprella bidentata Utinomi, 1947 (Amphipoda: Caprellidea), a synonym of Caprella monoceros Mayer, 1890, supported by experimental evidence. J Crustacean Biol 10:537–543

    Google Scholar 

  • Arimoto I (1976) Taxonomic studies of caprellids (Crustacea, Amphipoda, Caprellidae) found in the Japanese adjacent waters. Special publications from the Seto Marine Biological Laboratory Series III, 1–299. Nippon Printing & Publishing Co, Ltd, Osaka

  • Ashton GV (2006) Distribution and dispersal of the non-native caprellid amphipod, Caprella mutica Schurin 1935. Dissertation, University of Aberdeen

  • Ashton GV, Boos K, Shucksmith R, Cook E (2006) Rapid assessment of the distribution of marine non-native species in marinas in Scotland. Aquat Invasions 1:209–213

    Google Scholar 

  • Ashton GV, Stevens MI, Hart MC, Green DH, Burrows MT, Cook EJ, Willis KJ (2008) Mitochondrial DNA reveals multiple Northern Hemisphere introductions of Caprella mutica (Crustacea, Amphipoda). Mol Ecol 17:1293–1303

    CAS  PubMed  Google Scholar 

  • Audet D, Davis DS, Miron G, Moriyasu M, Benhalima K, Campbell R (2003) Geographical expansion of a nonindigenous crab, Carcinus maenas (L.), along the Nova Scotian shore into the southeastern Gulf of St Lawrence, Canada. J Shellfish Res 22:255–262

    Google Scholar 

  • Baeza-Rojano E, Calero-Cano S, Hachero-Cruzado I, Guerra-García JM (2013) A preliminary study of the Caprella scaura amphipod culture for potential use in aquaculture. J Sea Res 83:146–151

    Google Scholar 

  • Baird HP, Miller KJ, Stark J (2011) Evidence of hidden biodiversity, ongoing speciation and diverse patterns of genetic structure in giant Antartic amphipods. Mol Ecol 20:3439–3454

    PubMed  Google Scholar 

  • Bakir K, Katagan T (2011) On the occurrence of Caprella scaura Templeton, 1836 (Crustacea: Amphipoda) in Turkish waters. Zool Middle East 52:125–126

    Google Scholar 

  • Barrowclough GF, Zink RM (2009) Funds enough, and time: mtDNA, nuDNA and the discovery of divergence. Mol Ecol 18:2934–2936

    CAS  Google Scholar 

  • Cabezas MP, Guerra-García JM, Baeza-Rojano E, Redondo-Gómez S, Figueroa ME, Luque T, García-Gómez JC (2010) Exploring molecular variation in the cosmopolitan Caprella penantis (Crustacea: Amphipoda): results from RAPD analysis. J Mar Biol Assoc UK 90:617–622

    CAS  Google Scholar 

  • Cabezas MP, Cabezas P, Machordom A, Guerra-García JM (2013a) Hidden diversity and cryptic speciation refute cosmopolitan distribution in Caprella penantis (Crustacea: Amphipoda: Caprellidae). J Zool Syst Evol Res 51:85–99

    Google Scholar 

  • Cabezas MP, Navarro-Barranco C, Ros M, Guerra-García JM (2013b) Long-distance dispersal, low connectivity and molecular evidence of a new cryptic species in the obligate rafter Caprella andreae Mayer, 1890 (Crustacea: Amphipoda: Caprellidae). Helgol Mar Res 67:483–497

    Google Scholar 

  • Carlton JT (1996) Marine bioinvasions: the alternation of marine ecosystems by nonindigenous species. Oceanography 9:36–43

    Google Scholar 

  • Carlton JT, Eldredge LG (2009) Marine bioinvasions of Hawai‘i: the introduced and cryptogenic marine and estuarine animals and plants of the Hawaiian archipelago. Bishop Museum Press, Honolulu, Hawaii

  • Castilla JC, Lagos NA, Cerda M (2004) Marine ecosystem engineering by the alien ascidian Pyura praeputialis on a mid-intertidal rocky shore. Mar Ecol Prog Ser 268:119–130

    Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    CAS  PubMed  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    CAS  PubMed  Google Scholar 

  • Cockman B, Albone P (1987) Caprellidae of the Swan River estuary. In: John J (ed) Swan River estuary, ecology and management, Curtin University, Environmental Studies Group report no. 1. Curtin University of Technology, Perth, Australia, pp 163–177

  • Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–558

    CAS  PubMed  Google Scholar 

  • Coll M, Piroddi C, Steenbeek J, Kaschner K, Ben Rais Lasram F, Aguzzi J, Ballesteros E, Bianchi CN et al (2010) The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS One 5(8):e11842. doi:10.1371/journal.pone.0011842

    PubMed Central  PubMed  Google Scholar 

  • Concepcion GT, Kahng SE, Crepeau MW, Franklin EC, Coles SL, Toonen RJ (2010) Resolving natural ranges and marine invasions in a globally distributed octocoral (genus Carijoa). Mar Ecol Prog Ser 401:113–127

    Google Scholar 

  • Conner JK, Hartl DL (2004) A primer of ecological genetics. Sinauer & Associates, Sunderland

    Google Scholar 

  • Cook EJ, Jahnke M, Kerckhof F, Minchin D, Faasse M, Boos K, Ashton G (2007) European expansion of the introduced amphipod Caprella mutica Schurin 1935. Aquat Invasions 2:411–421

    Google Scholar 

  • Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystems engineers. Oikos 97:153–166

    Google Scholar 

  • Davies N, Villablanca FX, Roderick GK (1999) Determining the source of the individuals: multilocus genotyping in nonequilibrium population genetics. Trends Ecol Evol 14:17–21

    PubMed  Google Scholar 

  • Dougherty C, Steinberg JE (1953) Notes on the skeleton shrimps (Crustacea, Caprellidea) of California. Proc Biol Soc Wash 66:39–50

    Google Scholar 

  • Duda TF (1994) Genetic population structure of the recently introduced Asian clam, Potamocorbula amurensis, in San Francisco Bay. Mar Biol 119:235–241

    Google Scholar 

  • EU (2008) Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008 establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive). Off J EU L 164:19–40

    Google Scholar 

  • EU (2011) Communication from the Commission to the Council, the European Parliament, the European Economic and Social Committee and the Committee of the Regions: our life insurance, our natural capital: an EU biodiversity strategy to 2020. COM/2011/244. Brussels, European Commission

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    PubMed  Google Scholar 

  • Excoffier L, Smouse P, Quattro J (1992) Analyses of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed Central  PubMed  Google Scholar 

  • Facon B, Pointier JP, Jarne P, Sarda V, David P (2008) High genetic variance in life-history strategies within invasive populations by way of multiple introductions. Curr Biol 18:363–367

    CAS  PubMed  Google Scholar 

  • Ficetola GF, Bonin A, Miaud C (2008) Population genetics reveals origin and number of founders in a biological invasion. Mol Ecol 17:773–782

    CAS  PubMed  Google Scholar 

  • Floerl O, Inglis GJ (2005) Starting the invasion pathway: the interaction between source populations and human transport vectors. Biol Invasions 7:589–606

    Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Foster JM, Heard RW, Knott DM (2004) Northern range extensions from Caprella scaura Templeton, 1836 (Crustacea: Amphipoda: Caprellidae) on the Florida Gulf Coast and in South Carolina. Gulf Caribb Res 16:65–69

    Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed Central  PubMed  Google Scholar 

  • Galil BS (2007) Loss or gain? Invasive aliens and biodiversity in the Mediterranean Sea. Mar Pollut Bull 55:314–322

    CAS  PubMed  Google Scholar 

  • Galil BS, Occhipinti-Ambrogi A, Gollasch S (2008) Biodiversity impacts of species introductions via marine vessels. In: Abdulla A, Linden O (eds) Maritime traffic effects on biodiversity in the Mediterranean Sea: review of impacts, priority areas and mitigation measures. IUCN Centre for Mediterranean Cooperation, Malaga, pp 117–157

    Google Scholar 

  • GISD (2012) Global invasive species database. http://www.issg.org/database/species/ecology.asp?si=102&fr=1&sts=sss&lang=EN

  • Gollasch S (2002) The importance of ship hull fouling as a vector for species introduction into the North Sea. Biofouling 18:105–121

    Google Scholar 

  • Grabowski M, Rewicz T, Bacela-Spychalska K, Konopacka A, Mamos T, Jazdzewski K (2012) Cryptic invasion of Baltic lowlands by freshwater amphipod of Pontic origin. Aquat Invasions 7:337–346

    Google Scholar 

  • Guerra-García JM (2003) The Caprellidea (Crustacea: Amphipoda) from Mauritius Island, Western Indian Ocean. Zootaxa 232:1–24

    Google Scholar 

  • Guerra-García JM, Thiel M (2001) La fauna de caprélidos (Crustacea: Amphipoda: Caprellidea) de la costa de Coquimbo, centro-norte de Chile, con una clave taxonómica para la identificación de especies. Rev Chil Hist Nat 74:873–883

    Google Scholar 

  • Guerra-García JM, Ros M, Dugo-Cota A, Burgos V, Flores-León AM, Baeza-Rojano E, Cabezas MP, Núñez J (2011) Geographical expansion of the invader Caprella scaura (Crustacea: Amphipoda: Caprellidae) to the East Atlantic coast. Mar Biol 158:2617–2622

    Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3-0. Syst Biol 59:307–321

    CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hampton JO, Spencer PBS, Alpers DL, Twigg LE, Woolnough AP, Doust J (2004) Molecular techniques, wildlife management and the important of genetic population structure and dispersal: a case study with feral pigs. J Appl Ecol 41:735–743

    CAS  Google Scholar 

  • Hänfling B, Carvalho GR, Brandl R (2002) mt-DNA sequences and possible invasion pathways of the Chinese mitten crab. Mar Ecol Prog Ser 238:307–310

    Google Scholar 

  • Harrison RJ (1940) On the biology of the Caprellidae. Growth and moulting of Pseudoprotella phasma Montagu. J Mar Biol Assoc UK 24:483–493

    Google Scholar 

  • Hart MW, Sunday J (2007) Things fall apart: biological species form unconnected parsimony networks. Biol Lett 3:509–512

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hartl DL, Clark AG (1997) Principles of population genetics. Sinauer Associates, Sunderland

    Google Scholar 

  • Haydar D (2012) What is natural? The scale of cryptogenesis in the North Atlantic Ocean. Divers Distrib 18:101–110

    Google Scholar 

  • Holland BS (2000) Genetics of marine bioinvasions. Hydrobiologia 420:63–71

    CAS  Google Scholar 

  • Hou Z, Li S (2010) Intraspecific or interspecific variation: delimitation of species boundaries within the genus Gammarus (Crustacea, Amphipoda, Gammaridae), with description of four new species. Zool J Linn Soc Lon 160:215–253

    Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    CAS  PubMed  Google Scholar 

  • Johnson LE, Ricciardi A, Carlton JT (2001) Overland dispersal of aquatic invasive species: a risk assessment of transient recreational boating. Ecol Appl 11:1789–1799

    Google Scholar 

  • Kaluza P, Kölzsch A, Gastner MT, Blasius B (2010) The complex network of global cargo ship movements. J R Soc Interface 7:1093–1103

    PubMed Central  PubMed  Google Scholar 

  • Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kolbe JJ, Larson A, Losos JB (2007) Differential admixture shapes morphological variation among invasive populations of the lizard Anolis sagrei. Mol Ecol 16:1579–1591

    CAS  PubMed  Google Scholar 

  • Krapp T, Lang C, Libertini A, Melzer RR (2006) Caprella scaura Templeton, 1836 sensu lato (Amphipoda: Caprellidae) in the Mediterranean. 6. Org Divers Evol 6(Electr Suppl 3):1–18

    Google Scholar 

  • Laubitz DR (1970) Studies on the Caprellidae (Crustacea, Amphipoda) of the American North Pacific. Publ Océanogr Biol Natl Mus Nat Sci (Can) 1:1–89

    Google Scholar 

  • Laubitz DR (1995) Caprellidea (Crustacea: Amphipoda) from the southern and western Indian Ocean. Mésogée 54:81–100

    Google Scholar 

  • Lefébure T, Douady CJ, Gouy M, Gibert J (2006) Relationship between morphological taxonomy and molecular divergence within Crustacea: proposal of a molecular threshold to help species delimitation. Mol Ecol 40:435–447

    Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    CAS  PubMed  Google Scholar 

  • Lim STA, Alexander CG (1986) Reproductive behaviour of the caprellid amphipod Caprella scaura typica Mayer, 1890. Mar Behav Physiol 12:217–230

    Google Scholar 

  • Martínez J, Adarraga I (2008) First record of invasive caprellid Caprella scaura Templeton, 1836 sensu lato (Crustacea: Amphipoda: Caprellidae) from the Iberian Peninsula. Aquat Invasions 3:165–171

    Google Scholar 

  • Mayer P (1890) Die Caprelliden des Golfes von Neapel und der angrenzenden Meeres Abschnitte. Fauna und Flora des Golfes von Neapel 17:1–55

    Google Scholar 

  • Mayer P (1903) Die Caprelliden der Siboga-Expedition. Siboga Exped 34:1–160

    Google Scholar 

  • McCain JC (1968) The Caprellidae (Crustacea: Amphipoda) of the Western North Atlantic. Bull US Natl Mus 278:1–147

    Google Scholar 

  • McCain JC, Steinberg JE (1970) Amphipoda-I, Caprellidea-I. In: Gruner HE, Holthuis LB (eds) Crustaceorum catalogus 2. Dr. W. Junk Publishers, The Hague, The Netherlands, pp 1–78

  • Minchin D, Floerl O, Savini D, Occhipinti-Ambrogi A (2006) Small craft and the spread of exotic species. In: Davenport J, Davenport JD (eds) The ecology of transportation: managing mobility for the environment. Springer, Dortdrecht, NL, pp 99–118

  • Minchin D, Lodola A, Occhipinti-Ambrogi A (2012) The occurrence of Caprella scaura (Amphipoda: Caprellidae) in marinas in Lanzarote Island (Canary Archipelago, Macaronesia). Mar Biodivers Rec 5:1–5

    Google Scholar 

  • Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492

    Google Scholar 

  • Montelli L (2010) The recent geographical expansion of Caprella californica (Caprellidea: Caprellidae) around the coastline of Australia. Biol Invasions 12:725–728

    Google Scholar 

  • Mori A, Yamato S (1993) Caprella simia Mayer, 1903 (Crustacea: Amphipoda: Caprellidae) collected from the body surface of a frogfish Antennarius striatus (Shaw & Nodder, 1794). Nnmki-Seiburu 35:41–46

    Google Scholar 

  • Myers JH, Simberloff D, Kuris AM, Carey JR (2000) Eradication revisited: dealing with exotic species. Trends Ecol Evol 15:316–320

    PubMed  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Occhipinti-Ambrogi A (2000) Biotic invasions in a Mediterranean lagoon. Biol Invasions 2:165–176

    Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    CAS  PubMed  Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer v1.4. http://beast.bio.ed.ac.uk/Tracer

  • Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100

    CAS  PubMed  Google Scholar 

  • Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225

    Google Scholar 

  • Rius M, Pascual M, Turon X (2008) Phylogeography of the widespread marine invader Microcosmus squamiger (Ascidacea) reveals high genetic diversity of introduced populations and non-independent colonizations. Divers Distrib 14:818–828

    Google Scholar 

  • Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464

    PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    CAS  PubMed  Google Scholar 

  • Ros M, Guerra-García JM (2012) On the occurrence of the tropical caprellid Paracaprella pusilla Mayer, 1890 (Crustacea: Amphipoda) in Europe. Mediterr Mar Sci 13:134–139

    Google Scholar 

  • Ros M, Vázquez-Luis M, Guerra-García JM (2013a) The tropical caprellid amphipod Paracaprella pusilla: a new alien crustacean in the Mediterranean Sea. Helgol Mar Res. doi:10.1007/s10152-013-0353-4

    Google Scholar 

  • Ros M, Guerra-García JM, González-Macías M, Saavedra A, López-Fe CM (2013b) Influence of fouling communities on the establishment success of alien caprellids (Crustacea: Amphipoda) in Southern Spain. Mar Biol Res 9:261–273

    Google Scholar 

  • Ros M, Guerra-García JM, Navarro-Barranco C, Cabezas MP, Vázquez-Luis M (2014) The spreading of the non-native caprellid (Crustacea: Amphipoda) Caprella scaura Templeton, 1836 into southern Europe and northern Africa: a complicated taxonomy history. Mediterr Mar Sci 15:145–155

    Google Scholar 

  • Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632

    Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Google Scholar 

  • Schulz MK, Alexander CG (2001) Aggressive behaviour of Caprella scaura typica Mayer, 1890. (Crustacea: Amphipoda). Mar Freshw Behav Physiol 34:181–187

    Google Scholar 

  • Sconfietti R, Danesi P (1996) Variazioni strutturali in comunità di peracaridi agli estremi opposti del bacino di Malamocco (Laguna di Venezia). Soc Ital Ecol, Atti 17:407–410

    Google Scholar 

  • Sconfietti R, Mangili F, Savini D, Occhipinti-Ambrogi A (2005) Diffusion of the alien species Caprella scaura Templeton, 1836 (Amphipoda: Caprellidae) in the Northern Adriatic Sea. Biol Mar Mediterr 12:335–337

    Google Scholar 

  • Serejo CS (1998) Gammaridean and caprellidean fauna (Crustacea) associated with the sponge Dysidea fragilis Johnston at Arraial de Cabo, Rio de Janeiro, Brazil. Bull Mar Sci 63:363–385

    Google Scholar 

  • Simon-Bouhet B, Garcia-Meunier P, Viard F (2006) Multiple introductions promote range expansion of the mollusk Cyclope neritea (Nasariidae) in France: evidence from mitochondrial sequence data. Mol Ecol 15:1699–1711

    CAS  PubMed  Google Scholar 

  • Souissi JB, Kahri C, Salem MB, Zaouali J (2010) Les espèces non indigènes du macrobenthos des lagunes du sud-est Tunisien: point sur la situation. Rapports de la Commission Intérnationale pour l’Exploration Scientifique de la Mer Méditerranée 39:449

    Google Scholar 

  • Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M, Halpern BS, Jorge MA, Lomaba AL, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57(7):573–583

    Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    CAS  PubMed  Google Scholar 

  • Stimpson W (1857) The Crustacea and Echinodermata of the Pacific shores of North America. Boston J Nat Hist 6:503–513

    Google Scholar 

  • Takeuchi I, Hirano R (1995) Clinging behavior of the epifaunal caprellids (Amphipoda) inhabiting the Sargassum zone on the Pacific coast of Japan, with its evolutionary implications. J Crustacean Biol 15:481–492

    Google Scholar 

  • Takeuchi I, Oyamada A (2013) Description of two species of Caprella (Crustacea: Amphipoda: Caprellidae) from the North Pacific; C. californica Stimpson, 1857 and C. scauroides Mayer, 1903, with a new appraisal of species ranking for C. scauroides. Helgol Mar Res 67:371–381

    Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumer S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    CAS  PubMed Central  PubMed  Google Scholar 

  • Templeton R (1836) Descriptions of some undescribed exotic Crustacea. Trans Entomol Soc Lond 1:185–198

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensivity of progressive multiple sequence alignment through sequence weighting, position-specific gal penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000) Reduced genetic variation and the success of an invasive species. Proc Natl Acad Sci USA 97:5948–5953

    CAS  PubMed Central  PubMed  Google Scholar 

  • Utinomi H (1947) Caprellidea of Japan and adjacent waters. Seibutu Suppl 1:68–82

    Google Scholar 

  • Whiting MF (2002) Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zool Scr 1:93–104

    Google Scholar 

  • Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Annu Rev Ecol Evol Syst 38:327–359

    Google Scholar 

  • Witt JDS, Threloff DL, Hebert PDN (2006) DNA barcoding reveals extraordinary cryptic diversity in an amphipod genus: implications for desert spring conservation. Mol Ecol 15:3073–3082

    CAS  PubMed  Google Scholar 

  • Xavier R, Santos AM, Lima FP, Branco M (2009) Invasion or invisibility: using genetic and distributional data to investigate the alien or indigenous status of the Atlantic populations of the peracarid isopod, Stenosoma nadejda (Rezig 1989). Mol Ecol 18:3283–3290

    CAS  PubMed  Google Scholar 

  • Xavier R, Zenboudji S, Lima FP, Harris DJ, Santos AM, Branco M (2011) Phylogeography of the marine isopod Stenosoma nadejda (Rezig, 1989) in North African Atlantic and western Mediterranean coasts reveals complex differentiation patterns and a new species. Biol J Linn Soc 104:419–431

    Google Scholar 

  • Zardus JD, Hadfield MG (2005) Multiple origins and incursions of the Atlantic barnacle Chthamalus proteus in the Pacific. Mol Ecol 14:3719–3733

    CAS  PubMed  Google Scholar 

  • Zenetos A, Vassilopoulou V, Salomidi M, Poursanidis D (2008) Additions to the marine alien fauna of Greek waters (2007 update). Mar Biodivers Rec 1:1–8

    Google Scholar 

  • Zenetos A, Gofas S, Verlaque M, Cinar ME, García-Raso JE, Bianchi CN, Morri C, Azzurro E, Bilecenoglu M, Froglia C, Sioku I, Violanti D, Sfriso A, San-Martin G, Giangrande A, Katagan T, Ballesteros E, Ramos-Espla A, Mastrototaro F, Ocaña O, Zingone A, Gambi MC, Streftaris N (2010) Alien species in the Mediterranean Sea by 2010. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part I. Spatial distribution. Mediterr Mar Sci 11:381–493

    Google Scholar 

  • Zhan A, Macisaac HJ, Cristescu ME (2010) Invasion genetics of the Ciona intestinalis species complex: from regional endemism to global homogeneity. Mol Ecol 19:4678–4694

    CAS  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thanks to Macarena Ros, Carlos Navarro-Barranco and Elena Baeza-Rojano for their kind help and assistance during field work. Special thanks to N. L. Demchenko (CSJAP, Japan), L. Hughes (CSAUS, Australia), C. d’Udekem d’Acoz (CSGRE, Greece), J. Nuñez (CSTEN, Tenerife), C. S. Serejo and M. B. Lacerda (CSBRA, Brazil), R. A. King and D. N. Knott (CSCHA, Charleston), L. Montelli (CCWAU, Australia), and the California Academy of Sciences Invertebrate Zoology (San Francisco, CA) (CCSFB, CCSFE) for providing some of the samples used in the present study. Financial support of this work was provided by the Ministerio de Economía y Competitividad (Project CGL2011-22474, internal reference 2011-707) co-financed by FEDER funds of the European Union, by the Consejería de Economía, Innovación, Ciencia y Empleo, Junta de Andalucía (Project P11-RNM-7041) and FCT: PTDC/MAR/104169/2008. R. Xavier and M. Branco have FCT Grants with references SFRH/BPD/75851/2011 and SFRH/BPD/40073/2007, respectively. M. P. Cabezas was supported by a PhD Grant ‘III Plan Propio de Investigación’, from the University of Seville.

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Authors and Affiliations

  1. Laboratorio de Biología Marina, Departamento de Zoología, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012, Seville, Spain

    M. Pilar Cabezas & José Manuel Guerra-García

  2. CIBIO, Centro de Investigaçaõ em Biodiversidade e Recursos Genéticos, Campus Agrário de Vairão, 4485-661, Vairão, Portugal

    M. Pilar Cabezas, Raquel Xavier, Madalena Branco & António M. Santos

  3. School of Biological Sciences, Cardiff University, Cardiff, CF10 3AX, UK

    Raquel Xavier

  4. Departamento de Biologia, Faculdade de Ciências da Universidade do Porto, R. Campo Alegre, s/n, 4169-007, Porto, Portugal

    António M. Santos

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  1. M. Pilar Cabezas
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  2. Raquel Xavier
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  3. Madalena Branco
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  4. António M. Santos
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  5. José Manuel Guerra-García
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Correspondence to M. Pilar Cabezas.

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Cabezas, M.P., Xavier, R., Branco, M. et al. Invasion history of Caprella scaura Templeton, 1836 (Amphipoda: Caprellidae) in the Iberian Peninsula: multiple introductions revealed by mitochondrial sequence data. Biol Invasions 16, 2221–2245 (2014). https://doi.org/10.1007/s10530-014-0660-y

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  • DOI: https://doi.org/10.1007/s10530-014-0660-y

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